Cargando…

Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice

The gut microbiome is a dynamic community that significantly affects host health; it is frequently disturbed by medications such as antibiotics. Recently, probiotics have been proposed as a remedy for antibiotic-induced dysbiosis, but the efficacy of such treatments remains uncertain. Thus, the effe...

Descripción completa

Detalles Bibliográficos
Autores principales: Ojima, Miriam N., Gotoh, Aina, Takada, Hiromi, Odamaki, Toshitaka, Xiao, Jin-Zhong, Katoh, Toshihiko, Katayama, Takane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314955/
https://www.ncbi.nlm.nih.gov/pubmed/32625197
http://dx.doi.org/10.3389/fmicb.2020.01349
_version_ 1783550162545672192
author Ojima, Miriam N.
Gotoh, Aina
Takada, Hiromi
Odamaki, Toshitaka
Xiao, Jin-Zhong
Katoh, Toshihiko
Katayama, Takane
author_facet Ojima, Miriam N.
Gotoh, Aina
Takada, Hiromi
Odamaki, Toshitaka
Xiao, Jin-Zhong
Katoh, Toshihiko
Katayama, Takane
author_sort Ojima, Miriam N.
collection PubMed
description The gut microbiome is a dynamic community that significantly affects host health; it is frequently disturbed by medications such as antibiotics. Recently, probiotics have been proposed as a remedy for antibiotic-induced dysbiosis, but the efficacy of such treatments remains uncertain. Thus, the effect of specific antibiotic-probiotic combinations on the gut microbiome and host health warrants further research. We tested the effect vancomycin, amoxicillin, and ciprofloxacin on mice. Antibiotic administration was followed by one of the following recovery treatments: Bifidobacterium bifidum JCM 1254 as a probiotic (PR); fecal transplant (FT); or natural recovery (NR). Each antibiotic administration and recovery treatment was repeated three times over 9 weeks. We used the Shannon Index and Chao1 Index to determine gut microbiome diversity and assessed recovery by quantifying the magnitude of microbial shift using the Bray-Curtis Index of Dissimilarity. We determined the community composition by sequencing the V3–V4 regions of the 16S ribosomal RNA gene. To assess host health, we measured body weight and cecum weight, as well as mRNA expression of inflammation-related genes by reverse-transcription quantitative PCR. Our results show that community response varied by the type of antibiotic used, with vancomycin having the most significant effects. As a result, the effect of probiotics and fecal transplants also varied by antibiotic type. For vancomycin, the first antibiotic disturbance substantially increased the relative abundance of inflammatory species in the phylum Proteobacteria, such as Proteus, but the effect of subsequent disturbances was less pronounced, suggesting that the gut microbiome is affected by past disturbance events. Furthermore, although gut microbiome diversity did not recover, probiotic supplementation was effective in limiting cecum size enlargement and colonic inflammation caused by vancomycin. However, for amoxicillin and ciprofloxacin, the relative abundances of proinflammatory species were not greatly affected, and consequently, the effect of probiotic supplementation on community structure, cecum weight, and expression of inflammation-related genes was comparatively negligible. These results indicate that probiotic supplementation is effective, but only when antibiotics cause proinflammatory species-induced gut inflammation, suggesting that the necessity of probiotic supplementation is strongly influenced by the type of disturbance introduced to the community.
format Online
Article
Text
id pubmed-7314955
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-73149552020-07-02 Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice Ojima, Miriam N. Gotoh, Aina Takada, Hiromi Odamaki, Toshitaka Xiao, Jin-Zhong Katoh, Toshihiko Katayama, Takane Front Microbiol Microbiology The gut microbiome is a dynamic community that significantly affects host health; it is frequently disturbed by medications such as antibiotics. Recently, probiotics have been proposed as a remedy for antibiotic-induced dysbiosis, but the efficacy of such treatments remains uncertain. Thus, the effect of specific antibiotic-probiotic combinations on the gut microbiome and host health warrants further research. We tested the effect vancomycin, amoxicillin, and ciprofloxacin on mice. Antibiotic administration was followed by one of the following recovery treatments: Bifidobacterium bifidum JCM 1254 as a probiotic (PR); fecal transplant (FT); or natural recovery (NR). Each antibiotic administration and recovery treatment was repeated three times over 9 weeks. We used the Shannon Index and Chao1 Index to determine gut microbiome diversity and assessed recovery by quantifying the magnitude of microbial shift using the Bray-Curtis Index of Dissimilarity. We determined the community composition by sequencing the V3–V4 regions of the 16S ribosomal RNA gene. To assess host health, we measured body weight and cecum weight, as well as mRNA expression of inflammation-related genes by reverse-transcription quantitative PCR. Our results show that community response varied by the type of antibiotic used, with vancomycin having the most significant effects. As a result, the effect of probiotics and fecal transplants also varied by antibiotic type. For vancomycin, the first antibiotic disturbance substantially increased the relative abundance of inflammatory species in the phylum Proteobacteria, such as Proteus, but the effect of subsequent disturbances was less pronounced, suggesting that the gut microbiome is affected by past disturbance events. Furthermore, although gut microbiome diversity did not recover, probiotic supplementation was effective in limiting cecum size enlargement and colonic inflammation caused by vancomycin. However, for amoxicillin and ciprofloxacin, the relative abundances of proinflammatory species were not greatly affected, and consequently, the effect of probiotic supplementation on community structure, cecum weight, and expression of inflammation-related genes was comparatively negligible. These results indicate that probiotic supplementation is effective, but only when antibiotics cause proinflammatory species-induced gut inflammation, suggesting that the necessity of probiotic supplementation is strongly influenced by the type of disturbance introduced to the community. Frontiers Media S.A. 2020-06-18 /pmc/articles/PMC7314955/ /pubmed/32625197 http://dx.doi.org/10.3389/fmicb.2020.01349 Text en Copyright © 2020 Ojima, Gotoh, Takada, Odamaki, Xiao, Katoh and Katayama. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ojima, Miriam N.
Gotoh, Aina
Takada, Hiromi
Odamaki, Toshitaka
Xiao, Jin-Zhong
Katoh, Toshihiko
Katayama, Takane
Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title_full Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title_fullStr Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title_full_unstemmed Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title_short Bifidobacterium bifidum Suppresses Gut Inflammation Caused by Repeated Antibiotic Disturbance Without Recovering Gut Microbiome Diversity in Mice
title_sort bifidobacterium bifidum suppresses gut inflammation caused by repeated antibiotic disturbance without recovering gut microbiome diversity in mice
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314955/
https://www.ncbi.nlm.nih.gov/pubmed/32625197
http://dx.doi.org/10.3389/fmicb.2020.01349
work_keys_str_mv AT ojimamiriamn bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT gotohaina bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT takadahiromi bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT odamakitoshitaka bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT xiaojinzhong bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT katohtoshihiko bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice
AT katayamatakane bifidobacteriumbifidumsuppressesgutinflammationcausedbyrepeatedantibioticdisturbancewithoutrecoveringgutmicrobiomediversityinmice